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Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta.

Giani VC, Yamaguchi E, Boyle MJ, Seaver EC - Evodevo (2011)

Bottom Line: Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells.It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Kewalo Marine Laboratory, PBRC/University of Hawaii, 41 Ahui St,, Honolulu, HI 96813, USA. seaver@hawaii.edu.

ABSTRACT

Background: Stem cells have a critical role during adult growth and regeneration. Germline stem cells are specialized stem cells that produce gametes during sexual reproduction. Capitella teleta (formerly Capitella sp. I) is a polychaete annelid that reproduces sexually, exhibits adult growth and regeneration, and thus, is a good model to study the relationship between somatic and germline stem cells.

Results: We characterize expression of the two C. teleta orthologs of piwi, genes with roles in germline development in diverse organisms. Ct-piwi1 and Ct-piwi2 are expressed throughout the life cycle in a dynamic pattern that includes both somatic and germline cells, and show nearly identical expression patterns at all stages examined. Both genes are broadly expressed during embryonic and larval development, gradually becoming restricted to putative primordial germ cells (PGCs) and the posterior growth zone. In juveniles, Ct-piwi1 is expressed in the presumptive gonads, and in reproductive adults, it is detected in gonads and the posterior growth zone. In addition, Ct-piwi1 is expressed in a population of putative PGCs that persist in sexually mature adults, likely in a stem cell niche. Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.

Conclusions: In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells. It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

No MeSH data available.


Phylogenetic analysis of Ct-Piwi1 and Ct-Piwi2 sequences. The argonaute and piwi subfamilies are indicated by a red and blue line, respectively. Ct-Piwi1 and Ct-Piwi2 are both members of the Piwi subfamily of Argonaute proteins. Ct-Piwi2 clusters in a sub-group, indicated by a green line, containing other Piwi2 or Piwi-like proteins from broad metazoan taxa. The tree shown is a Bayesian consensus tree with posterior probabilities placed above the nodes. Maximum likelihood bootstrap support values are included where the tree topology agreed with the Bayesian analysis, and are placed below the nodes. Species abbreviations: Amphi, Branchiostoma floridae; Bm, Bombyx mori; Ce, Caenorhabditis elegans; Ct-, Capitella teleta; Ci-, Ciona intestinalis; Che, Clytia hemisphaerica; Dm, Drosophila melanogaster; Hro-, Helobdella robusta; Hs, Homo sapiens; Lg, Lottia gigantea; Mm, Mus musculus; Nv, Nematostella vectensis; Pdu-, Platynereis dumerilii; Pc, Podocoryne carnea; Sp, Strongylocentrotus purpuratus. JGI protein ID number is indicated for C. teleta outgroup and sequences from H. robusta, L. gigantea, and N. vectensis. NCBI accession number is indicated for C. intestinalis. Gene locus number is indicated for B. floridae.
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Figure 1: Phylogenetic analysis of Ct-Piwi1 and Ct-Piwi2 sequences. The argonaute and piwi subfamilies are indicated by a red and blue line, respectively. Ct-Piwi1 and Ct-Piwi2 are both members of the Piwi subfamily of Argonaute proteins. Ct-Piwi2 clusters in a sub-group, indicated by a green line, containing other Piwi2 or Piwi-like proteins from broad metazoan taxa. The tree shown is a Bayesian consensus tree with posterior probabilities placed above the nodes. Maximum likelihood bootstrap support values are included where the tree topology agreed with the Bayesian analysis, and are placed below the nodes. Species abbreviations: Amphi, Branchiostoma floridae; Bm, Bombyx mori; Ce, Caenorhabditis elegans; Ct-, Capitella teleta; Ci-, Ciona intestinalis; Che, Clytia hemisphaerica; Dm, Drosophila melanogaster; Hro-, Helobdella robusta; Hs, Homo sapiens; Lg, Lottia gigantea; Mm, Mus musculus; Nv, Nematostella vectensis; Pdu-, Platynereis dumerilii; Pc, Podocoryne carnea; Sp, Strongylocentrotus purpuratus. JGI protein ID number is indicated for C. teleta outgroup and sequences from H. robusta, L. gigantea, and N. vectensis. NCBI accession number is indicated for C. intestinalis. Gene locus number is indicated for B. floridae.

Mentions: Searches of the C. teleta genome identified two putative piwi homologs, which we call Ct-piwi1 and Ct-piwi2. Both predicted open reading frames contain conserved PAZ and PIWI domains characteristic of piwi genes. The PIWI domain in both Ct-Piwi1 and Ct-Piwi2 is located near the 3' end of the ORF, which is typical of piwi genes [25]. Phylogenetic analyses were conducted by Bayesian and maximum likelihood methods. Both Ct-Piwi1 and Ct-Piwi2 cluster within the Piwi subfamily of the Ago family of proteins, separately from the Argonaute subfamily (Figure 1). There is 100% Bayesian posterior probability support for the Piwi subfamily node, as well as 100% maximum likelihood bootstrap support. Ct-Piwi1 and Ct-Piwi2 are more closely related to Piwi paralogs from other animals than to each other; we infer that these two genes do not represent a recent gene duplication. Indeed, most of the animals included in these analyses have at least two paralogs that are divergent from each other, which suggests a deep root for this duplication, perhaps in the bilaterian or even metazoan ancestor. While there is some lack of resolution among the Piwi1, Piwi-like1, Piwi-like3, and Piwi-like4 proteins, the Piwi2 and Piwi-like2 sequences group closely together, with 100% Bayesian posterior probability support and 97% maximum likelihood bootstrap support for this node. Ct-Piwi2 belongs to this Piwi2 sub-group, which includes representatives from a broad range of metazoan taxa.


Somatic and germline expression of piwi during development and regeneration in the marine polychaete annelid Capitella teleta.

Giani VC, Yamaguchi E, Boyle MJ, Seaver EC - Evodevo (2011)

Phylogenetic analysis of Ct-Piwi1 and Ct-Piwi2 sequences. The argonaute and piwi subfamilies are indicated by a red and blue line, respectively. Ct-Piwi1 and Ct-Piwi2 are both members of the Piwi subfamily of Argonaute proteins. Ct-Piwi2 clusters in a sub-group, indicated by a green line, containing other Piwi2 or Piwi-like proteins from broad metazoan taxa. The tree shown is a Bayesian consensus tree with posterior probabilities placed above the nodes. Maximum likelihood bootstrap support values are included where the tree topology agreed with the Bayesian analysis, and are placed below the nodes. Species abbreviations: Amphi, Branchiostoma floridae; Bm, Bombyx mori; Ce, Caenorhabditis elegans; Ct-, Capitella teleta; Ci-, Ciona intestinalis; Che, Clytia hemisphaerica; Dm, Drosophila melanogaster; Hro-, Helobdella robusta; Hs, Homo sapiens; Lg, Lottia gigantea; Mm, Mus musculus; Nv, Nematostella vectensis; Pdu-, Platynereis dumerilii; Pc, Podocoryne carnea; Sp, Strongylocentrotus purpuratus. JGI protein ID number is indicated for C. teleta outgroup and sequences from H. robusta, L. gigantea, and N. vectensis. NCBI accession number is indicated for C. intestinalis. Gene locus number is indicated for B. floridae.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 1: Phylogenetic analysis of Ct-Piwi1 and Ct-Piwi2 sequences. The argonaute and piwi subfamilies are indicated by a red and blue line, respectively. Ct-Piwi1 and Ct-Piwi2 are both members of the Piwi subfamily of Argonaute proteins. Ct-Piwi2 clusters in a sub-group, indicated by a green line, containing other Piwi2 or Piwi-like proteins from broad metazoan taxa. The tree shown is a Bayesian consensus tree with posterior probabilities placed above the nodes. Maximum likelihood bootstrap support values are included where the tree topology agreed with the Bayesian analysis, and are placed below the nodes. Species abbreviations: Amphi, Branchiostoma floridae; Bm, Bombyx mori; Ce, Caenorhabditis elegans; Ct-, Capitella teleta; Ci-, Ciona intestinalis; Che, Clytia hemisphaerica; Dm, Drosophila melanogaster; Hro-, Helobdella robusta; Hs, Homo sapiens; Lg, Lottia gigantea; Mm, Mus musculus; Nv, Nematostella vectensis; Pdu-, Platynereis dumerilii; Pc, Podocoryne carnea; Sp, Strongylocentrotus purpuratus. JGI protein ID number is indicated for C. teleta outgroup and sequences from H. robusta, L. gigantea, and N. vectensis. NCBI accession number is indicated for C. intestinalis. Gene locus number is indicated for B. floridae.
Mentions: Searches of the C. teleta genome identified two putative piwi homologs, which we call Ct-piwi1 and Ct-piwi2. Both predicted open reading frames contain conserved PAZ and PIWI domains characteristic of piwi genes. The PIWI domain in both Ct-Piwi1 and Ct-Piwi2 is located near the 3' end of the ORF, which is typical of piwi genes [25]. Phylogenetic analyses were conducted by Bayesian and maximum likelihood methods. Both Ct-Piwi1 and Ct-Piwi2 cluster within the Piwi subfamily of the Ago family of proteins, separately from the Argonaute subfamily (Figure 1). There is 100% Bayesian posterior probability support for the Piwi subfamily node, as well as 100% maximum likelihood bootstrap support. Ct-Piwi1 and Ct-Piwi2 are more closely related to Piwi paralogs from other animals than to each other; we infer that these two genes do not represent a recent gene duplication. Indeed, most of the animals included in these analyses have at least two paralogs that are divergent from each other, which suggests a deep root for this duplication, perhaps in the bilaterian or even metazoan ancestor. While there is some lack of resolution among the Piwi1, Piwi-like1, Piwi-like3, and Piwi-like4 proteins, the Piwi2 and Piwi-like2 sequences group closely together, with 100% Bayesian posterior probability support and 97% maximum likelihood bootstrap support for this node. Ct-Piwi2 belongs to this Piwi2 sub-group, which includes representatives from a broad range of metazoan taxa.

Bottom Line: Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells.It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Kewalo Marine Laboratory, PBRC/University of Hawaii, 41 Ahui St,, Honolulu, HI 96813, USA. seaver@hawaii.edu.

ABSTRACT

Background: Stem cells have a critical role during adult growth and regeneration. Germline stem cells are specialized stem cells that produce gametes during sexual reproduction. Capitella teleta (formerly Capitella sp. I) is a polychaete annelid that reproduces sexually, exhibits adult growth and regeneration, and thus, is a good model to study the relationship between somatic and germline stem cells.

Results: We characterize expression of the two C. teleta orthologs of piwi, genes with roles in germline development in diverse organisms. Ct-piwi1 and Ct-piwi2 are expressed throughout the life cycle in a dynamic pattern that includes both somatic and germline cells, and show nearly identical expression patterns at all stages examined. Both genes are broadly expressed during embryonic and larval development, gradually becoming restricted to putative primordial germ cells (PGCs) and the posterior growth zone. In juveniles, Ct-piwi1 is expressed in the presumptive gonads, and in reproductive adults, it is detected in gonads and the posterior growth zone. In addition, Ct-piwi1 is expressed in a population of putative PGCs that persist in sexually mature adults, likely in a stem cell niche. Ct-piwi1 is expressed in regenerating tissue, and once segments differentiate, it becomes most prominent in the posterior growth zone and immature oocytes in regenerating ovaries of regenerating segments.

Conclusions: In C. teleta, piwi genes may have retained an ancestral role as genetic regulators of both somatic and germline stem cells. It is likely that piwi genes, and associated stem cell co-regulators, became restricted to the germline in some taxa during the course of evolution.

No MeSH data available.